, Volume 16, Issue 3, pp 891–900 | Cite as

Long-Term Follow-up in Patients with Spontaneous Intracerebral Hemorrhage Treated With or Without Surgical Intervention: a Large-Scale Retrospective Study

  • XianXiu Chen
  • Yuan-Chih Su
  • Chun-Chung Chen
  • Jeng-Hung Guo
  • Chih-ying Wu
  • Sung-Tai Wei
  • Der-Cherng Chen
  • Jung-Ju Lin
  • Shwn-Huey Shieh
  • Cheng-Di ChiuEmail author
Original Article


Debates regarding the most beneficial medical or surgical procedures for patients with spontaneous intracerebral hemorrhage (sICH) are still ongoing. We aimed to evaluate the risk of subsequent vascular disease and mortality in patients with sICH treated with and without surgical intervention, in a large-scale Asian population. Patients hospitalized within 2000 to 2013 who were newly diagnosed with sICH were identified using the National Health Insurance Research Database of Taiwan. Neuroendoscopy and craniotomy groups comprised patients who underwent surgical treatment within 1 week, while those in the control group did not undergo early surgical treatment. Outcomes included subsequent hemorrhagic and ischemic stroke, following acute myocardial infarction, congestive heart failure, and mortality. After propensity score matching, there were 663 patients in each group. Compared to that in the control group, the neuroendoscopy and craniotomy groups had a significantly higher risk of secondary vascular events at 1 to 3 months of follow-up (adjusted HR, 2.08 and 1.95; 95% CI, 1.21–3.58 and 1.13–3.35; p < 0.01 and p < 0.05, respectively), but a significantly lower risk after 3 years of follow-up (adjusted HR, 0.52 and 0.52; 95% CI, 0.35–0.78 and 0.35–0.77; p < 0.01 and p < 0.01, respectively). The mortality rate was higher in the craniotomy group at 6 to 12 months of follow-up (adjusted HR, 2.18; 95% CI, 1.06–4.49; p < 0.05) compared to that in the control group. Thus, a timely surgical intervention for hematoma evacuation is advantageous in preventing secondary vascular events and improving outcomes in the long term. However, greater attention to secondary ischemic stroke following the initial sICH episode is needed.

Key Words

Spontaneous intracerebral hemorrhage neuroendoscopy craniotomy subsequent vascular risk stroke mortality 



This study was supported by the China Medical University Hospital (DMR-105-054) and was partially supported by the Taiwan Ministry of Health and Welfare Clinical Trial Center (MOHW108-TDU-B-212-133004); China Medical University Hospital; Academia Sinica Stroke Biosignature Project (BM10701010021); MOST Clinical Trial Consortium for Stroke (MOST 107-2321-B-039-004); Tseng-Lien Lin Foundation, Taichung, Taiwan; Katsuzo and Kiyo Aoshima Memorial Funds, Japan; and the “Chinese Medicine Research Center, China Medical University,” from the Featured Areas Research Center Program within the framework of the Higher Education Sprout Project by the Ministry of Education (MOE) in Taiwan (CMRC-CMA-7).

Role of the Funder/Sponsor

The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Required Author Forms

Disclosure forms provided by the authors are available with the online version of this


Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflicts of interest.

Supplementary material

13311_2019_722_MOESM1_ESM.pdf (498 kb)
ESM 1 (PDF 498 kb)


  1. 1.
    van Asch CJ, Luitse MJ, Rinkel GJ, van der Tweel I, Algra A, Klijn CJ. Incidence, case fatality, and functional outcome of intracerebral haemorrhage over time, according to age, sex, and ethnic origin: a systematic review and meta-analysis. Lancet Neurol 2010;9:167–176.CrossRefGoogle Scholar
  2. 2.
    Poon MT, Fonville AF, Al-Shahi Salman R. Long-term prognosis after intracerebral haemorrhage: systematic review and meta-analysis. J Neurol Neurosurg Psychiatry 2014;85:660–667.CrossRefGoogle Scholar
  3. 3.
    Anderson CS, Huang Y, Wang JG, et al. Intensive blood pressure reduction in acute cerebral haemorrhage trial (INTERACT): a randomised pilot trial. Lancet Neurol 2008;7:391–399.CrossRefGoogle Scholar
  4. 4.
    Feigin VL, Forouzanfar MH, Krishnamurthi R, et al. Global and regional burden of stroke during 1990-2010: findings from the Global Burden of Disease Study 2010. Lancet 2014;383:245–254.CrossRefGoogle Scholar
  5. 5.
    Richard F Keep Y, Guohua Xi. Intracerebral haemorrhage: mechanisms of injury and therapeutic targets. Lancet Neurol 2012;11:720–731.CrossRefGoogle Scholar
  6. 6.
    Kaya RA, Turkmenoglu O, Ziyal IM, Dalkilic T, Sahin Y, Aydin Y. The effects on prognosis of surgical treatment of hypertensive putaminal hematomas through transsylvian transinsular approach. Surg Neurol 2003;59:176–183; discussion 83.CrossRefGoogle Scholar
  7. 7.
    Li Q, Yang CH, Xu JG, Li H, You C. Surgical treatment for large spontaneous basal ganglia hemorrhage: retrospective analysis of 253 cases. Br J Neurosurg 2013;27:617–621.CrossRefGoogle Scholar
  8. 8.
    Background: National Health Insurance Research Database. Center for Biomedical Resources of NHRI. (Accessed 23 January 2017, at
  9. 9.
    Hsiao FY YC, Huang YT, Huang WF. Using Taiwan’s National Health Insurance Research Databases for Pharmacoepidemiology Research. J Food Drug Anal 2007;15:99–108.Google Scholar
  10. 10.
    Huang WF, Hsiao FY, Wen YW, Tsai YW. Cardiovascular events associated with the use of four nonselective NSAIDs (etodolac, nabumetone, ibuprofen, or naproxen) versus a cyclooxygenase-2 inhibitor (celecoxib): a population-based analysis in Taiwanese adults. Clin Ther 2006;28:1827–1836.CrossRefGoogle Scholar
  11. 11.
    Yang SY, Kao Yang YH, Chong MY, Yang YH, Chang WH, Lai CS. Risk of extrapyramidal syndrome in schizophrenic patients treated with antipsychotics: a population-based study. Clin Pharmacol Ther 2007;81:586–594.CrossRefGoogle Scholar
  12. 12.
    Suzanne L. West MER, Charles Poole. Validity of Pharmacoepidemiologic Drug and Diagnosis Data: John Wiley & Sons, Ltd. Hoboken, 2013.Google Scholar
  13. 13.
    Fisher ES, Whaley FS, Krushat WM, et al. The accuracy of Medicare’s hospital claims data: progress has been made, but problems remain. Am J Public Health 1992;82:243–248.CrossRefGoogle Scholar
  14. 14.
    Cheng CL, Kao YH, Lin SJ, Lee CH, Lai ML. Validation of the National Health Insurance Research Database with ischemic stroke cases in Taiwan. Pharmacoepidemiol Drug Saf 2011;20:236–242.CrossRefGoogle Scholar
  15. 15.
    Broderick J, Connolly S, Feldmann E, et al. Guidelines for the management of spontaneous intracerebral hemorrhage in adults: 2007 update: a guideline from the American Heart Association/American Stroke Association Stroke Council, High Blood Pressure Research Council, and the Quality of Care and Outcomes in Research Interdisciplinary Working Group. Circulation 2007;116:e391-e413.CrossRefGoogle Scholar
  16. 16.
    Mendelow AD, Gregson BA, Fernandes HM, et al. Early surgery versus initial conservative treatment in patients with spontaneous supratentorial intracerebral haematomas in the International Surgical Trial in Intracerebral Haemorrhage (STICH): a randomised trial. Lancet 2005;365:387–397.CrossRefGoogle Scholar
  17. 17.
    Mendelow AD, Gregson BA, Rowan EN, et al. Early surgery versus initial conservative treatment in patients with spontaneous supratentorial lobar intracerebral haematomas (STICH II): a randomised trial. Lancet 2013;382:397–408.CrossRefGoogle Scholar
  18. 18.
    Hanley DF, Thompson RE, Muschelli J, et al. Safety and efficacy of minimally invasive surgery plus alteplase in intracerebral haemorrhage evacuation (MISTIE): a randomised, controlled, open-label, phase 2 trial. Lancet Neurol 2016;15:1228–1237.CrossRefGoogle Scholar
  19. 19.
    Mould WA, Carhuapoma JR, Muschelli J, et al. Minimally invasive surgery plus recombinant tissue-type plasminogen activator for intracerebral hemorrhage evacuation decreases perihematomal edema. Stroke 2013;44:627–634.CrossRefGoogle Scholar
  20. 20.
    Spiotta AM, Fiorella D, Vargas J, et al. Initial multicenter technical experience with the Apollo device for minimally invasive intracerebral hematoma evacuation. Neurosurgery 2015;11 Suppl 2:243–251; discussion 51.CrossRefGoogle Scholar
  21. 21.
    Przybylowski CJ, Ding D, Starke RM, Webster Crowley R, Liu KC. Endoport-assisted surgery for the management of spontaneous intracerebral hemorrhage. J Clin Neurosci 2015;22:1727–1732.CrossRefGoogle Scholar
  22. 22.
    Egashira Y, Hua Y, Keep RF, Xi G. Intercellular cross-talk in intracerebral hemorrhage. Brain Res 2015;1623:97–109.Google Scholar
  23. 23.
    Aronowski J, Zhao X. Molecular pathophysiology of cerebral hemorrhage: secondary brain injury. Stroke 2011;42:1781–1786.CrossRefGoogle Scholar
  24. 24.
    Arboix A, Comes E, Garcia-Eroles L, et al. Site of bleeding and early outcome in primary intracerebral hemorrhage. Acta Neurol Scand 2002;105:282–288.CrossRefGoogle Scholar
  25. 25.
    Broderick JP. The STICH trial: what does it tell us and where do we go from here? Stroke 2005;36:1619–1620.CrossRefGoogle Scholar
  26. 26.
    Ye Z, Ai X, Hu X, Fang F, You C. Comparison of neuroendoscopic surgery and craniotomy for supratentorial hypertensive intracerebral hemorrhage: A meta-analysis. Medicine 2017;96:e7876.CrossRefGoogle Scholar
  27. 27.
    Prabhakaran S, Naidech AM. Ischemic brain injury after intracerebral hemorrhage: a critical review. Stroke 2012;43:2258–2263.CrossRefGoogle Scholar

Copyright information

© The American Society for Experimental NeuroTherapeutics, Inc. 2019

Authors and Affiliations

  • XianXiu Chen
    • 1
    • 2
  • Yuan-Chih Su
    • 3
    • 4
  • Chun-Chung Chen
    • 3
    • 5
    • 6
  • Jeng-Hung Guo
    • 5
  • Chih-ying Wu
    • 5
    • 7
  • Sung-Tai Wei
    • 5
  • Der-Cherng Chen
    • 5
  • Jung-Ju Lin
    • 8
  • Shwn-Huey Shieh
    • 9
  • Cheng-Di Chiu
    • 5
    • 6
    • 10
    Email author
  1. 1.Chinese Medicine Research CenterChina Medical UniversityTaichungTaiwan
  2. 2.Research Center for Chinese Herbal MedicineChina Medical UniversityTaichungTaiwan
  3. 3.School of MedicineChina Medical UniversityTaichungTaiwan
  4. 4.Management Office for Health DataChina Medical University HospitalTaichungTaiwan
  5. 5.Department of NeurosurgeryChina Medical University HospitalTaichungTaiwan
  6. 6.Stroke CenterChina Medical University HospitalTaichungTaiwan
  7. 7.The Graduate Institute of Integrated MedicineChina Medical UniversityTaichungTaiwan
  8. 8.Department of Internal MedicineChina Medical University HospitalTaichungTaiwan
  9. 9.Department of Health Services AdministrationChina Medical UniversityTaichungTaiwan
  10. 10.Graduate Institute of Biomedical ScienceChina Medical UniversityTaichungTaiwan

Personalised recommendations